Philopatric reproduction, a prime mover in the evolution of termite sociality?

Abstract

Philopatric reproduction commonly occurs even in the most basic isopteran lineages and is almost certainly a primitive potentiality of these insects. Several authors hypothesized that opportunities for philopatric reproduction may have been a prime mover for the three most remarkable events in the evolution of termite sociality: the origin of helping behaviour, the origin of soldiers, and the origin of a permanently apterous worker caste. A critical assessment of these hypotheses and a review of relevant evidence are presented here. I first discuss the hypothesis that termite helpers derive from individuals choosing to postpone dispersal because of nest inheritance prospects. Such individuals would have developed helping as a strategy yielding indirect reproductive benefits while they wait for reproductive opportunities. However, it appears that prospects of philopatric reproduction need not be invoked to explain the origin of helping behaviour, which can be justified more parsimoniously by a favourable intrinsic benefit/cost ratio. Second, the hypothesis that soldiers originated through selection for fighting abilities among neotenic reproductives is found to face important difficulties, the major one being how to explain the absence of fighting devices in almost all presentday neotenics. Finally, the hypothesized link between apterism and chances of philopatric reproduction, which might have favoured the onset of the worker caste, is poorly supported by empirical evidence. It appears thus that philopatric reproduction, notwithstanding its importance in the biology of many extant termite species, is unlikely to have been a prime mover in the evolution of helping and of altruistic castes in termites.

Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis

“…For example, Z. nevadensis alates appear to outbreed (Shellman-Reeve 2001) but secondary reproductives are common in Zootermopsis colonies that have lost one or both primaries (Castle 1934;Light & Illg 1945), probably reducing allelic variation in their offspring (Husseneder et al 1999;Thorne et al 1999;Vargo 2003;DeHeer & Vargo 2004). In addition, nesting ecology (Hamilton 1972), predation on alates (Lepage 1991;Matsuura & Nishida 2002) and disease risk (Rosengaus & Traniello 1993;Rosengaus et al 2000;Calleri et al 2005) may limit dispersal, which could also increase inbreeding (Roisin 1999). Cycles of inbreeding and outbreeding may have influenced the way in which termite colonies adapted to disease, outbreeding generating variation in disease resistance traits and inbreeding maintaining adapted disease-resistant genotypes selected for during colony growth (Thorne & Traniello 2003).…”

Delayed dispersal as a potential route to cooperative breeding in ambrosia beetles

“…However, eusociality has been discovered in a variety of widely distinct taxa (see Aoki 1977;Alexander et al 1991;Kent and Simpson 1992;Crespi 1992;Duffy 1996;Thorne 1997), many of which are not haplodiploid. Therefore, there is increasing interest to develop a general framework of social evolution that includes both invertebrates and vertebrates (Roisin 1999). Most research on the evolution of social systems has focused on variation of phenotypes within social species.…”

Evolution of eusociality and the soldier caste in termites: Influence of intraspecific competition and accelerated inheritance

“…Kin selection is less potent in these groups that lack relatedness asymmetries between sexes and generations, indicating that other factors must also be important in explaining eusociality (3,4,14,16,17). Previous nonmutually exclusive theories regarding the evolution of eusociality in termites (4,(17)(18)(19)(20)(21)(22) have been constructive but indecisive; the current consensus is that termite eusocial evolution was driven by a suite of selective forces (4,17,21,23).…”

“…The inheritance hypothesis, productively applied to the evolution of altruistic behavior in other social groups, was logically extended to termites, supported by the fact that philopatric reproduction is common through helper differentiation into secondary (replacement or supplementary) reproductives on death or senescence of established reproductives (4,17,26). An apparent problem with this application to termites, however, is that founding kings and queens are long-lived in captivity and in some field colonies (31), even in relatively primitive taxa (32), suggesting that early orphaning of helpers (or originally, nonhelpers) and thus opportunities for inheritance might be rare in the young families that must have characterized the evolutionary transition to termite eusociality (23). Founder life spans may have been shorter in prototermites than in modern groups (4), but timing of inheritance opportunities would be important if parents survived past the time their first offspring could reach sexual maturity and if remaining in the natal nest resulted in progeny delaying or forgoing direct reproduction.…”